Complex heterochrony underlies the evolution of hermaphrodite self-fertility and sex allocation in experimental C. elegans populations

Abstract

AbstractHermaphroditic organisms are common both in plants and animals, and have served as key models to study the evolution of sex allocation. Despite extensive past research, the specific developmental mechanisms by which hermaphrodite sex allocation can evolve remain largely unknown. To address this problem, we here use experimental evolution of Caenorhabditis elegans hermaphrodite-male populations to directly quantify changes in germline and somatic development that underlie adaptive shifts in hermaphrodite sex allocation associated with the evolution of improved self-fertility. Specifically, we test whether the evolution of hermaphrodite sex allocation is due to heterochrony, i.e. evolutionary changes in the relative timing of developmental processes.We show that the experimental evolution of improved hermaphrodite self-fertility occurred through complex modification of a suite of developmental and reproductive traits: increased sperm production, accelerated oogenesis and ovulation rates, and increased embryo retention in utero. The experimental evolution of increased sperm production delayed entry into oogenesis – as expected, given the sequentially coupled production of spermatogenesis and oogenesis. Surprisingly, however, delayed oogenesis onset did not delay reproductive maturity, nor did it trade-off with gamete or embryo size. Comparing developmental dynamics of germline and soma indicates that the evolution of increased sperm production did not delay reproductive maturity due to a globally accelerated larval development during the period of spermatogenesis.We conclude that the integration of multiple heterochronic events in gametogenesis and soma can explain the experimental evolution of hermaphrodite sex allocation and self-fertility. Our results thus support the idea that heterochrony can represent a specific mechanism that explains the maintenance of partial selfing in natural populations with mixed reproduction modes and different forms of hermaphroditism. More generally, our results provide a quantitative perspective on how natural selection can operate on developmental characters – and their integration – during the evolution of life history at the population level.